Cathepsin S regulates class II MHC processing in human CD4+ HLA-DR+ T cells

Journal of Immunology

Volumn 183, Issue 2, 2009, Pages 945-952

  Costantino, Cristina Maria ^a   Ploegh, Hidde L ^b   Hafler, David A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHEPSIN S; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN; PROTEIN CLIP; UNCLASSIFIED DRUG; AUTOANTIGEN; B LYMPHOCYTE ANTIGEN; CATHEPSIN; HLA ANTIGEN CLASS 2; PEPTIDE HYDROLASE;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; EX VIVO STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE CLONE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REGULATORY MECHANISM; CELL CLONE; ENZYMOLOGY; GENETICS; IMMUNOLOGY; INVARIANT CHAIN; LYMPHOCYTE ACTIVATION; LYSOSOME; METABOLISM; PHYSIOLOGY;

ANTIGEN PRESENTATION; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; AUTOANTIGENS; B-LYMPHOCYTES; CATHEPSINS; CD4-POSITIVE T-LYMPHOCYTES; CLONE CELLS; DOWN-REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-DR ANTIGENS; HUMANS; LYMPHOCYTE ACTIVATION; LYSOSOMES; PEPTIDE HYDROLASES;

EID: 70249099290     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900921     Document Type: Article

References (47)

1. Evans, R. L., T. J. Faldetta, R. E. Humphreys, D. M. Pratt, E. J. Yunis, and S. F. Schlossman. 1978. Peripheral human T cells sensitized in mixed leukocyte culture synthesize and express Ia-like antigens. J. Exp. Med. 148: 1440-1445.
2. Ko, H. S., S. M. Fu, R. J. Winchester, D. T. Yu, and H. G. Kunkel. 1979. Ia determinants on stimulated human T lymphocytes. Occurrence on mitogen- and antigen-activated T cells. J. Exp. Med. 150: 246-255.
3. Holling, T. M., E. Schooten, and P. J. van Den Elsen. 2004. Function and regulation of MHC class II molecules in T-lymphocytes: of mice and men. Hum. Immunol. 65: 282-290.
4. Chang, C. H., S. C. Hong, C. C. Hughes, C. A. Janeway, Jr., and R. A. Flavell. 1995. CIITA activates the expression of MHC class II genes in mouse T cells. Int. Immunol. 7: 1515-1518.
5. Holling, T. M., N. van der Stoep, E. Quinten, and P. J. van den Elsen. 2002. Activated human T cells accomplish MHC class II expression through T cell-specific occupation of class II transactivator promoter III. J. Immunol. 168: 763-770.
6. Yu, D. T., R. J. Winchester, S. M. Fu, A. Gibofsky, H. S. Ko, and H. G. Kunkel. 1980. Peripheral blood Ia-positive T cells. Increases in certain diseases and after immunization. J. Exp. Med. 151: 91-100.
7. LaSalle, J. M., K. Ota, and D. A. Hafler. 1991. Presentation of autoantigen by human T cells. J. Immunol. 147: 774-780.
8. Wucherpfennig, K. W., P. Hollsberg, J. H. Richardson, D. Benjamin, and D. A. Hafler. 1992. T-cell activation by autologous human T-cell leukemia virus type I-infected T-cell clones. Proc. Natl. Acad. Sci. USA 89: 2110-2114.
9. Lanzavecchia, A., E. Roosnek, T. Gregory, P. Berman, and S. Abrignani. 1988. T cells can present antigens such as HIV gp120 targeted to their own surface molecules. Nature 334: 530-532.
10. Baecher-Allan, C., E. Wolf, and D. A. Hafler. 2006. MHC class II expression identifies functionally distinct human regulatory T cells. J. Immunol. 176: 4622-4631.
11. Bryant, P., and H. Ploegh. 2004. Class II MHC peptide loading by the professionals. Curr. Opin. Immunol. 16: 96-102.
12. Denzin, L. K., and P. Cresswell. 1995. HLA-DM induces CLIP dissociation from MHC class II α β dimers and facilitates peptide loading. Cell 82: 155-165.
13. Nakagawa, T. Y., and A. Y. Rudensky. 1999. The role of lysosomal proteinases in MHC class II-mediated antigen processing and presentation. Immunol. Rev. 172: 121-129.
14. Villadangos, J. A., R. A. Bryant, J. Deussing, C. Driessen, A. M. Lennon-Dumenil, R. J. Riese, W. Roth, P. Saftig, G. P. Shi, H. A. Chapman, et al. 1999. Proteases involved in MHC class II antigen presentation. Immunol. Rev. 172: 109-120.
15. Brachet, V., G. Raposo, S. Amigorena, and I. Mellman. 1997. Ii chain controls the transport of major histocompatibility complex class II molecules to and from lysosomes. J. Cell Biol. 137: 51-65.
16. Neefjes, J. J., and H. L. Ploegh. 1992. Inhibition of endosomal proteolytic activity by leupeptin blocks surface expression of MHC class II molecules and their conversion to SDS resistance α β heterodimers in endosomes. EMBO J. 11: 411-416.
17. Riese, R. J., P. R. Wolf, D. Brömme, L. R. Natkin, J. A. Villadangos, H. L. Ploegh, and H. A. Chapman. 1996. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 4: 357-366.
18. Nakagawa, T., and A. Rudensky. 1998. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus. Science 4: 450-453.
19. Shi, G. P., R. A. Bryant, R. Riese, S. Verhelst, C. Driessen, Z. Li, D. Bromme, H. L. Ploegh, and H. A. Chapman. 2000. Role for cathepsin F in invariant chain processing and major histocompatibility complex class II peptide loading by macrophages. J. Exp. Med. 191: 1177-1186.
20. Biddison, W. E. 2001. Generation of continuously growing B cell lines by epstein-barr virus transformation. Curr. Protoc Cell Biol. Chapter 2: Unit 2 4.
21. Costantino, C. M., H. C. Hang, S. C. Kent, D. A. Hafler, and H. L. Ploegh. 2008. Lysosomal cysteine and aspartic proteases are heterogeneously expressed and act redundantly to initiate human invariant chain degradation. J. Immunol. 180: 2876-2885.
22. Kitamura, H., H. Kamon, S. Sawa, S. Park, N. Katunuma, K. Ishihara, M. Murakami, and T. Hirano. 2005. IL-6-STAT3 controls intracellular MHC class II αβ dimer level through cathepsin S activity in dendritic cells. Immunity 23: 491-502.
23. Maehr, R., H. C. Hang, J. D. Mintern, Y. M. Kim, A. Cuvillier, M. Nishimura, K. Yamada, K. Shirahama-Noda, I. Hara-Nishimura, and H. L. Ploegh. 2005. Asparagine endopeptidase is not essential for class II MHC antigen presentation but is required for processing of cathepsin L in mice. J. Immunol. 174: 7066-7074.
24. Hewitt, C. R., and M. Feldmann. 1989. Human T cell clones present antigen. J. Immunol. 143: 762-769.
25. Matsui, Y., H. M. Shapiro, M. J. Sheehy, L. Christenson, D. E. Staunton, E. E. Eynon, and E. J. Yunis. 1986. Differential expression of T cell differentiation antigens and major histocompatibility antigens on activated T cells during the cell cycle. Eur. J. Immunol. 16: 248-251.
26. Beck, H., G. Schwarz, C. J. Schroter, M. Deeg, D. Baier, S. Stevanovic, E. Weber, C. Driessen, and H. Kalbacher. 2001. Cathepsin S and an asparagine-specific endoprotease dominate the proteolytic processing of human myelin basic protein in vitro. Eur. J. Immunol. 31: 3726-3736.
27. Riese, R. J., R. N. Mitchell, J. A. Villadangos, G. P. Shi, J. T. Palmer, E. R. Karp, G. T. De Sanctis, H. L. Ploegh, and H. A. Chapman. 1998. Cathepsin S activity regulates antigen presentation and immunity. J. Clin. Invest. 101: 2351-2363.
28. Felbor, U., L. Dreier, R. A. Bryant, H. L. Ploegh, B. R. Olsen, and W. Mothes. 2000. Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J. 19: 1187-1194.
29. Palmer, J. T., D. Rasnick, J. L. Klaus, and D. Bromme. 1995. Vinyl sulfones as mechanism-based cysteine protease inhibitors. J. Med. Chem. 38: 3193-3196.
30. Trombetta, E. S., and I. Mellman. 2005. Cell biology of antigen processing in vitro and in vivo. Annu. Rev. Immunol. 23: 975-1028.
31. Brandes, M., K. Willimann, and B. Moser. 2005. Professional antigen-presentation function by human γδ T cells. Science 309: 264-268.
32. Oshima, S., and D. D. Eckels. 1990. Selective signal transduction through the CD3 or CD2 complex is required for class II MHC expression by human T cells. J. Immunol. 145: 4018-4025.
33. Lanzavecchia, A., and F. Sallusto. 2000. Dynamics of T lymphocyte responses: intermediates, effectors, and memory cells. Science 290: 92-97.
34. Fung-Leung, W. P., C. D. Surh, M. Liljedahl, J. Pang, D. Leturcq, P. A. Peterson, S. R. Webb, and L. Karlsson. 1996. Antigen presentation and T cell development in H2-M-deficient mice. Science 271: 1278-1281.
35. Martin, W. D., G. G. Hicks, S. K. Mendiratta, H. I. Leva, H. E. Ruley, and L. Van Kaer. 1996. H2-M mutant mice are defective in the peptide loading of class II molecules, antigen presentation, and T cell repertoire selection. Cell 84: 543-550.
36. Avva, R. R., and P. Cresswell. 1994. In vivo and in vitro formation and dissociation of HLA-DR complexes with invariant chain-derived peptides. Immunity 1: 763-774.
37. Mizuochi, T., S. T. Yee, M. Kasai, T. Kakiuchi, D. Muno, and E. Kominami. 1994. Both cathepsin B and cathepsin D are necessary for processing of ovalbumin as well as for degradation of class II MHC invariant chain. Immunol. Lett. 43: 189-193.
38. Honey, K., and A. Y. Rudensky. 2003. Lysosomal cysteine proteases regulate antigen presentation. Nat. Rev. Immunol. 3: 472-482.
39. Akari, H., Y. Goto, and T. Shinjo. 1995. Detection of the cellular membrane proteins on human T cell leukemia virus type I. Arch. Virol. 140: 375-382.
40. LaSalle, J. M., P. J. Tolentino, G. J. Freeman, L. M. Nadler, and D. A. Hafler. 1992. Early signaling defects in human T cells anergized by T cell presentation of autoantigen. J. Exp. Med. 176: 177-186.
41. Macon-Lemaitre, L., and F. Triebel. 2005. The negative regulatory function of the lymphocyte-activation gene-3 co-receptor (CD223) on human T cells. Immunology 115: 170-178.
42. Bulwin, G. C., S. Walter, M. Schlawinsky, T. Heinemann, A. Schulze, W. Hohne, G. Krause, W. Kalka-Moll, P. Fraser, H. D. Volk, J. Lohler, E. L. Milford, and N. Utku. 2008. HLA-DR α 2 mediates negative signalling via binding to Tirc7 leading to anti-inflammatory and apoptotic effects in lymphocytes in vitro and in vivo. PLoS ONE 3: e1576.
43. Lanzavecchia, A., S. Abrignani, D. Scheidegger, R. Obrist, B. Dorken, and G. Moldenhauer. 1988. Antibodies as antigens: the use of mouse monoclonal antibodies to focus human T cells against selected targets. J. Exp. Med. 167: 345-352.
44. Krogsgaard, M., J. Juang, and M. M. Davis. 2007. A role for "self" in T-cell activation. Semin. Immunol. 19: 236-244.
45. Röhn, T., M. Boes, D. Wolters, S. Spindeldreher, B. Müller, H. Langen, H. Ploegh, A. Vogt, and H. Kropshofer. 2004. Upregulation of the CLIP self peptide on mature dendritic cells antagonizes T helper type 1 polarization. Nat. Immunol. 5: 909-918.
46. Manoury, B., E. W. Hewitt, N. Morrice, P. M. Dando, A. J. Barrett, and C. Watts. 1998. An asparaginyl endopeptidase processes a microbial antigen for class II MHC presentation. Nature 396: 695-699.
47. Burster, T., A. Beck, E. Tolosa, V. Marin-Esteban, O. Rotzschke, K. Falk, A. Lautwein, M. Reich, J. Brandenburg, G. Schwarz, et al. 2004. Cathepsin G, and not the asparagine-specific endoprotease, controls the processing of myelin basic protein in lysosomes from human B lymphocytes. J. Immunol. 172: 5495-5503.